CROTCHETS & QUIDDITIES

Come to Me, My Melancholic Baby!KENNETH WEISS

There’s not much point in writ-ing a column about things wealready know, but there is value

in looking at things we thought wealready knew. One way to do this is tosee how textbooks illustrate basicprinciples. I was led to write this col-umn when my daughter took an intro-ductory bioanthropology course thisyear and asked me something aboutnatural selection. Her class had beendiscussing the example of industrialmelanism and the peppered moth. Ifound that curious, because I thoughtI had seen several years ago that thatexample had been undermined bycontradictory evidence from colorchanges in the same moths in NorthAmerica. How could it still be in text-books?

This brought to mind Stephen JayGould’s making fun in Natural Historyof the classic description of the earlyhorse Eohippus (or Hyracotherium) asbeing the size of a fox terrier (Figure1). This comparison was first used in1904 by the paleontologist H. F. Os-born in reconstructing horse evolu-tion. The simile was then copied fromtextbook to textbook by authors—andfor readers—who, like me, probablyhad little idea even what a fox terrierlooked like. And according to Gould,

the comparison was wrong. He saidthe horse was bigger. Of course, wehave to presume that he himself hadactually seen a fox terrier.

As so often happens, somethingsimilar came up coincidentally in anunrelated conversation, and is closerto anthropology. In 1940 the promi-nent geneticist A. H. Sturtevant sug-gested that tongue-rolling ability illus-trated the genetic control of humantraits, and we’ve used it as a classroomexample ever since (are you TT or tt?).It costs nothing to test in students,and if you assume a dominant gene inHardy-Weinberg equilibrium you canalways estimate the allele frequency.However, in 1965 Sturtevant retractedhis suggestion that the trait was ge-netic, saying “I am still embarrassedto see it listed in some current worksas an established Mendelian case.”Tongue rolling has still not been com-pletely displaced as a classroom ex-ample of Mendelian inheritance, butif it is genetic at all, it’s neither a sim-ple single-locus trait nor even a singlebiological trait, and may in fact besomething most people can acquireduring a critical developmental pe-riod.

These whimsical examples of text-book echoing illustrate Lewis Carroll’spromise in The Hunting of the Snarkthat “what I tell you three times istrue.” But this may not always be triv-ial, so it is worth looking at cases inwhich questions have been raisedabout the two classic examples usedto buttress core concepts of evolution-ary biology, which could have seriouspractical consequences if the exam-ples are wrong.

CATCHING EVOLUTIONIN THE ACT

Of Birds and Bugs

A quick check of the web confirmedmy recollection that numerous prob-lems had been raised about industrialmelanism as an example of naturalselection observed in action (andtouted by creationists as disprovingthe evolutionary edifice) (see Majerusand B. S. Grant references). What arethese issues?

In 1896 J. W. Tutt suggested protec-tive coloration against bird predationas an explanation of the rapid recentrise in the frequency of melanic formsof the peppered moth Biston betulariain Britain. The selective force was pre-dation facilitated by industrial air pol-lution. Most moths had been of thelight-colored typica form with blackspeckles, and enjoyed protective col-oration on lichen-covered trees wherethey were hard for birds to see, be-cause they dramatically resemble themottled pattern of lichens (Figure 2).But soot from the industrial revolu-tion blackened the trees in the 19thcentury, killed the lichens, and de-prived the moths of their protective

Ken Weiss is Evan Pugh Professor of An-thropology and Genetics at Penn Univer-sity.

Evolutionary Anthropology 12:3–6 (2003)DOI 10.1002/evan.10040Published online in Wiley InterScience(www.interscience.wiley.com).

Come to me, my melancholy baby,Cuddle up and like your hue . . .All your fears are foolish fancy,

maybeYou know dear, that I’ll be tree to

you.

Every smog may have a silver lining,But until the sun shines through,Smile, my honey dear,While I kiss away each tear,‘Cause I’ll be staying melancholic

too!’

Some famous textbook cases of evolution aren’t unambiguously true. Does itmatter?

Evolutionary Anthropology 3

cover. This favored a formerly raremelanic variant whose pepperingblack spots were so large that thewings were essentially all black, con-ferring reversed protective colorationagainst the newly blackened trees.The carbonaria form rose rapidly infrequency. As pollution waned afterClean Air Acts were passed in the 20thcentury, the variant frequencies re-verted towards the lighter pepperedform.

This selective hypothesis was exam-ined theoretically by the leading pop-ulation geneticist J. B. S. Haldane andothers in the 1920s. In the 1950s Ber-nard Kettlewell undertook a series offamous experiments to demonstrate itdirectly. Among other tests, he placedmoths on trees and observed crypticto non-cryptic predation rates bybirds. This became, and remains, theclassic direct demonstration of evolu-tion by natural selection. However,many aspects of this work have beenquestioned. I mention some of themto illustrate the problems.

To the human eye the mothsseemed to enjoy cryptic protection,but evidence suggests that birds cansee into the UV light spectrum, whichmeans that protective coloration maybe less effective to them than it is tothe scientists suggesting the hypothe-sis. Kettlewell performed his experi-ments under various artificial condi-tions. He used unnatural mothdensities in his experiments, and hereleased the moths in daylight, whenthey quickly landed on the nearest

(and hence most exposed) places onthe tree trunks; normally these mothshide in the branches, and are activeonly at night when birds aren’t. Ket-tlewell stressed the role of lichens be-cause they appeared to provide an ex-ceptionally cryptic background for thepeppered form, but there has been de-bate about whether moths preferen-tially seek lichens that match theirown color, which would obviate pre-dation based on color. Even the cor-relation of morph frequency with thepresence of lichens is imperfect inBritain, so geographic anomalies be-tween pollution and melanic fre-quency have had to be explained afterthe fact by invoking gene flow. There

is also evidence of differential mortal-ity in the expected direction, but ofpre-adult moths, which cannot be at-tributed to protective coloration. Fi-nally, I was able to confirm my recol-lection that there was a parallelchange in color variants in NorthAmerican moths, and parallel pat-terns of industrialization, but lichenswere not involved here and the changemay be continuing in regions that donot share comparable pollution differ-ences.

It is disturbing that so many aspectsof what seemed such a classically sim-ple exemplar of evolution could be cred-ibly questioned. However, it appearsthat the problems, though serious, donot entirely invalidate the story. If sootand lichens were not involved in thecolor pattern changes in North Amer-ica, there was a correlation here, as inBritain, with air pollutants like SO2 thataffect reflectance on trees. That’s notthe same as mimicking lichens, but it isa plausible source of protective colora-tion. Although several studies showingdifferential predation by birds of con-spicuous moths had various designproblems, their findings have been con-sistently in the expected direction. It isprobably true that protective colorationis at most one of several factors that willexplain this story. For example, the factthat color changes in two continentshave paralleled the history of air pollu-tion is compelling, but we have to be-ware that we not fall into the commontrap of equating correlation with causa-

Figure 1. Horse and Hounds? (Not to scale.) Courtesy www.nature.ca/nature_e.cfm andwww.akc.org.

Figure 2. Liking lichens? Kettlewall’s Biston betularia. Lichen covered tree with dark and light(lower left) variants. (From Kettlewell, 1956.)

4 Evolutionary Anthropology CROTCHETS & QUIDDITIES

tion. Air pollution has been associatedwith many things, and we may notknow them all.

Above all, however, the changes incolor frequency have been too rapid,widespread, and consistent to be dueto any known factor other than someform(s) of natural selection, whetheror not we know the exact factors in-volved. At the very least, the melanismstory does illustrate micro-evolution,even if this old chestnut of evolutionturns out to be more subtle than thesimple textbook tale.

To Speak of Beaks

The oddity of a brief episode of in-tense selection induced by human in-dustrial pollution may have parallelsin more “natural” natural selection.Climate change has also been involvedin another classic story, related to theevolution of Darwin’s famous Galapa-gos finches. These birds are so wellestablished as defining instances ofadaptive evolution that the GalapagosIslands are on the must see list of bi-ologists the way a hajj to Mecca is inIslam. Everyone knows that after ar-riving from South America the finchesevolved by adaptation to local condi-tions on the various islands. It is al-most mandatory to include this exam-ple even in anthropology textbooks.Darwin himself illustrated this adap-tive radiation with a drawing of theirbeak variation (Figure 3). But here,too, the story is not so simple, in in-teresting ways.

Over the past 30 years, Peter and

Rosemary Grant have observed theGalapagos finches in detail. Duringthis time there have been changes inclimate, including droughts that af-fect plant survival and hence the dis-tribution of available seed sizes. TheGrants systematically collected dataon survival and census counts of twospecies (Geospiza fortis, mediumground finch; and Geospiza scandens,cactus finch). They recently summa-rized the changes of body size, beaksize, and beak shape they observedover this period (Grant and Grant,2002). On the micro-evolutionaryscale, they provide elegant studies ofselection, as defined as statisticallysignificant change in trait frequenciesfrom one generation to the next, di-rectly observed in action.

A major finding was that selectionoccurred in repeated short bursts.When appropriate circumstances ex-isted, the birds showed the expectedfavorable relative survival of birdswith beak characteristics suited forthe seed size distribution that existedin a given year, and this really was“selection” in the evolutionary sensethat is, it changed the trait distribu-tions in the next generation. But thedirection, magnitude, and consistencyof these bursts varied among traitsand between the species. Stochastic(statistically nonsignificant) changesalso occurred, and traits also changedsignificantly over this period as a re-sult of hybridization and gene flow.There were reversals in the directionof selection, but they did not restore apopulation to its initial state at the

time their study began. Strong selec-tion in times of drought also did notexhaust variation, as was shown bythe birds’ ability to respond whenrains returned.

Overall, the phenotype changes orstates over these 30 years were notpredictable from the changes thatcould have been observed in a singleseason or short time span. For exam-ple, data from the first 5 years couldnot have been used in population ge-netics models to predict the 30-yearresults. Selection certainly occurs,and if your beak is too small you can’teat big tough seeds and won’t do wellif there aren’t any small seeds around.The Grants’ major point was a plea formore long-term observational studies,because typical small, short-term ob-servational studies may be insufficientto understand how evolution is actu-ally working. This is clearly appropri-ate, but there may be two deeperpoints. First, the kinds of traits Dar-win observed are still bouncingaround evolutionarily. How confi-dently can we infer the past selectiveforces that got the traits to where theyare (temporarily) today? And second,no observational study is long relativeto the evolutionary time scale, whichis often what we want to understand.Would even a 100 year study beenough?

COMPLEXITY BURIEDWITHIN SIMPLICITY

The true evolutionary story is morecomplex than the textbooks depictionof a long, steady convergence to anadaptive peak. To many biologists, itmay suffice just to know that selectioncan be demonstrated in the wild. Butit is at best less satisfying to have toinvoke constantly and rapidly chang-ing mixes of selective forces. We maybe getting at least the main selectivefactors right, but so many things inevolutionary biology dissolve on closeinspection, that I’ll be crotchety andask how we know that the other fac-tors were just nuisances, and that re-sults would have been the same if theyweren’t there. There are many prece-dents to give us pause about such anassumption.

Diethard Tautz (2000) has ex-pressed the challenge in a memorable

Figure 3. Darwin’s finches. (From Darwin’s The Voyage of the Beagle, 1845.)

CROTCHETS & QUIDDITIES Evolutionary Anthropology 5

way. The outcome of selection de-pends on its strength and duration,and on population size. If these fac-tors have roughly quantitatively com-parable impact, which may be the rulemore than the exception, evolutionaryoutcomes are fundamentally probabi-listic, which Tautz refers to as a “pop-ulation genetic uncertainty principle,”reminiscent of the Heisenberg princi-ple in physics. This could happen evenif selection were strong but irregularor episodic, or involved many compet-ing factors. To infer a selection regimeunder such conditions would requirestudies that were themselves on anevolutionary or species wide scale.

Butterflies That Won’t Migrateand Genes That Do?

These issues, of course, apply inprinciple to our need to explain hu-man and primate evolution from amix of fragmentary fossil data andshort-term observation, little if any ofit as clear as the situation in mothsand finches. But I think that morethan just the richness of the real evo-lutionary story is lost in the uncriticalrepetition of simplistic textbook ex-amples. The subtleties that actuallyoccur have implications for social pol-icy as can be seen by an example ofinterest to North American anthropol-ogists because it involves one of ourfavorite species: maize.

A few years ago it was reported thatpollen from genetically modified(GM) corn was dangerous to monarchbutterflies (Losey et al., 1999; Hansen-Jesse and Obrycki, 2000). This chal-lenged heavily vested interests, and re-sulted in several studies to see if thereports were true. Generally, the newstudies found little if any ill effects(Gatehouse et al., 2002). The originalfindings in part reflected the intensi-fied experimental exposures that wereapplied in order to get a useful resultin a reasonable time period. This hasbeen standard practice in testingdrugs or food additives in mice feddoses many times larger than any hu-man will normally consume, under

the conservative assumption thatharm is harm. That’s roughly compa-rable to extrapolating the results ofstrong short-term selection in finches,so can we trust the results even ofwell-done but necessarily short-termnatural-conditions field experiments?The issue is more than just academic,because transgenic insecticide genesmay already have escaped from do-mestic GM corn to wild maize in Oax-aca, Mexico, as was reported by an-other study (Chapela and Quist,2001). Despite some methodologicalproblems (Nature, April 11, 2002), theauthors maintain that their basic find-ing is true and it has been confirmed.If so, this will constitute evolution inaction, but how can we know whetherthis is something to be concernedabout?

Unfortunately, as I was finishingthis column the peppered moth storywas made the subject of highly publi-cized scandal-mongering, with theimplication that no evidence re-mained that industrial melanism wasan example of evolution in action (seeGrant, 2002). Sadly, this is likely tochange textbooks, which we can pre-dict will make much of the scandal,and that that, too will be repeatedfrom book to book. We can only hopethat despite the uncertainties the evi-dence that this is a documented evo-lutionary story will also proliferate.

It is important to raise all appropri-ate questions about dogma in science.That in both the cases of beaks andspots it has been shown directly thatselection works, and that we’ve prob-ably identified at least some of theforces, is a triumph of evolutionarybiology. But we should also smile andnot be melancholy that weaknesseshave been discovered. Weaknesses arenot failures. Digesting the messagethat evolution even in these classiccases is not so clear after all will leadto deeper understanding of evolutionand better applications to situationsthat may really matter, as the maizeexample may illustrate.

But rather than always having tofight rearguard actions in evolution-

ary biology, it would be nicer if all wehad to worry about were tiny horsesor rolled-up tongues.

NOTES

Send any comments on this columnto: kmw4@psu.edu. I maintain CrotchetyComments on my web page: www.anthro.psu.edu/rsrch/weiss lab.htm. Ithank Anne Buchanan, Sam Sholtis,and John Fleagle for critically readingthis manuscript; Bruce Grant for mothhelp; and Chris Carlson for pointing outthe tongue-rolling example.

My Melancholy Baby by E. Burnet,music; G. Norton, lyrics; 1912 (e.g.,http://home.swipnet.se/�w-134536/mel27.htm).

THINGS TO READ

Many things discussed here can beprofitably explored by web searching.Gateshouse AMR, Ferry N, Raemaekers RJM.2002. The case of the monarch butterfly: a verdict isreturned. Trends in Genetics 18: 249–251.Gould SJ. 1988. The case of the creeping foxterrier clone. Natural History 97: 16–24.Grant BS, Owen DF, Clarke CA, Owen DF. 1996.Parallel rise and fall of melanic peppered mothsin America and Britain. J Heredity 87: 351–357.Grant BS. 1999. Fine tuning the peppered mothparadigm. Evolution 53: 980–984.Grant BS, Wiseman LL. 2002. Recent history ofmelanism in American peppered moths. J Hered-ity 93: 86–90.Grant BS. 2002. Sour grapes of wrath. Science297: 941–942.Grant PR, Grant BR. 2002. Unpredictable evolu-tion in a 30-year study of Darwin’s finches. Sci-ence 296: 707–711.Hansen-Jesse LC, Obrycki JJ. 2000. Field deposi-tion of Bt transgenic corn pollen: lethal effects onthe monarch butterfly. Oecologia 125: 241–248.Kettlewell HBD. 1956. Further selection experi-ments on industrial melanism in the Lepidop-tera. Heredity 10: 287–301.Losey J, Rayer LS, Carter ME. 1999. Transgenicpollen harms monarch larvae. Nature 399: 214.Majerus MEN. 1998. Melanism-evolution in ac-tion. New York: Oxford University Press.Quist D, Chapela IH. 2001. Transgenic DNA in-trogressed into traditional maize landraces inOaxaca, Mexico. Nature 414: 541–543.Sturtevant AH. 1940. A new inherited characterin man. Proc Natl Acad Sci USA 26: 100–102.Sturtevant HA. 1965. A History of Genetics. NewYork: Harper and Row.Tautz D. 2000. A genetic uncertainty principle.Trends in Genetics 16: 475–477.Tutt JW. 1986. British Moths. London: Routledge.

© 2003 Wiley-Liss, Inc.

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